Distinct Mechanisms of Recognizing Endosomal Sorting Complex Required for Transport III (ESCRT-III) Protein IST1 by Different Microtubule Interacting and Trafficking (MIT) Domains

Guo, Emily Z.; Xu, Zhaohui

doi:10.1074/jbc.M114.607903

Title: Distinct Mechanisms of Recognizing Endosomal Sorting Complex Required for Transport III (ESCRT-III) Protein IST1 by Different Microtubule Interacting and Trafficking (MIT) Domains

Journal Article · Thu Feb 05 04:00:00 UTC 2015 · Journal of Biological Chemistry

DOI: https://doi.org/10.1074/jbc.M114.607903 · OSTI ID:1177441

Guo, Emily Z. ^[1]; Xu, Zhaohui ^[2]

Univ. of Michigan, Ann Arbor, MI (United States). Life Science Inst.
Univ. of Michigan, Ann Arbor, MI (United States). Medical School. Dept. of Biological Chemistry. Life Science Inst.

The endosomal sorting complex required for transport (ESCRT) machinery is responsible for membrane remodeling in a number of biological processes including multivesicular body biogenesis, cytokinesis, and enveloped virus budding. In mammalian cells, efficient abscission during cytokinesis requires proper function of the ESCRT-III protein IST1, which binds to the microtubule interacting and trafficking (MIT) domains of VPS4, LIP5, and Spartin via its C-terminal MIT-interacting motif (MIM). In this paper, we studied the molecular interactions between IST1 and the three MIT domain-containing proteins to understand the structural basis that governs pairwise MIT-MIM interaction. Crystal structures of the three molecular complexes revealed that IST1 binds to the MIT domains of VPS4, LIP5, and Spartin using two different mechanisms (MIM1 mode versus MIM3 mode). Structural comparison revealed that structural features in both MIT and MIM contribute to determine the specific binding mechanism. Within the IST1 MIM sequence, two phenylalanine residues were shown to be important in discriminating MIM1 versus MIM3 binding. Finally, these observations enabled us to deduce a preliminary binding code, which we applied to provide CHMP2A, a protein that normally only binds the MIT domain in the MIM1 mode, the additional ability to bind the MIT domain of Spartin in the MIM3 mode.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Univ. of Michigan, Ann Arbor, MI (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Inst. of Health (NIH) (United States); Michigan Economic Development Corp. (United States); Michigan Technology Tri-Corridor (United States)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1177441

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Journal Issue: 13 Vol. 290; ISSN 0021-9258

Publisher:: American Society for Biochemistry and Molecular BiologyCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (62)

The identification of a conserved domain in both spartin and spastin, mutated in hereditary spastic paraplegia Ciccarelli, Francesca D.; Proukakis, Christos; Patel, Heema Genomics, Vol. 81, Issue 4 https://doi.org/10.1016/S0888-7543(03)00011-9	journal	April 2003
Hereditary spastic paraplegia: clinical features and pathogenetic mechanisms Salinas, Sara; Proukakis, Christos; Crosby, Andrew The Lancet Neurology, Vol. 7, Issue 12 https://doi.org/10.1016/S1474-4422(08)70258-8	journal	December 2008
Escrt-III Babst, Markus; Katzmann, David J.; Estepa-Sabal, Eden J. Developmental Cell, Vol. 3, Issue 2 https://doi.org/10.1016/S1534-5807(02)00220-4	journal	August 2002
Functional Reconstitution of ESCRT-III Assembly and Disassembly Saksena, Suraj; Wahlman, Judit; Teis, David Cell, Vol. 136, Issue 1 https://doi.org/10.1016/j.cell.2008.11.013	journal	January 2009
Structural Basis for Budding by the ESCRT-III Factor CHMP3 Muzioł, Tadeusz; Pineda-Molina, Estela; Ravelli, Raimond B. Developmental Cell, Vol. 10, Issue 6 https://doi.org/10.1016/j.devcel.2006.03.013	journal	June 2006
Structural Basis of Vta1 Function in the Multivesicular Body Sorting Pathway Xiao, Junyu; Xia, Hengchuan; Zhou, Jiahai Developmental Cell, Vol. 14, Issue 1 https://doi.org/10.1016/j.devcel.2007.10.013	journal	January 2008
ESCRT-III Family Members Stimulate Vps4 ATPase Activity Directly or via Vta1 Azmi, Ishara F.; Davies, Brian A.; Xiao, Junyu Developmental Cell, Vol. 14, Issue 1 https://doi.org/10.1016/j.devcel.2007.10.021	journal	January 2008
MIT Domainia Hurley, James H.; Yang, Dong Developmental Cell, Vol. 14, Issue 1 https://doi.org/10.1016/j.devcel.2007.12.013	journal	January 2008
Two Distinct Modes of ESCRT-III Recognition Are Required for VPS4 Functions in Lysosomal Protein Targeting and HIV-1 Budding Kieffer, Collin; Skalicky, Jack J.; Morita, Eiji Developmental Cell, Vol. 15, Issue 1 https://doi.org/10.1016/j.devcel.2008.05.014	journal	July 2008
Ordered Assembly of the ESCRT-III Complex on Endosomes Is Required to Sequester Cargo during MVB Formation Teis, David; Saksena, Suraj; Emr, Scott D. Developmental Cell, Vol. 15, Issue 4 https://doi.org/10.1016/j.devcel.2008.08.013	journal	October 2008
The ESCRT Pathway Henne, William M.; Buchkovich, Nicholas J.; Emr, Scott D. Developmental Cell, Vol. 21, Issue 1 https://doi.org/10.1016/j.devcel.2011.05.015	journal	July 2011
Structural Basis for ESCRT-III CHMP3 Recruitment of AMSH Solomons, Julianna; Sabin, Charles; Poudevigne, Emilie Structure, Vol. 19, Issue 8 https://doi.org/10.1016/j.str.2011.05.011	journal	August 2011
Structural basis for selective recognition of ESCRT-III by the AAA ATPase Vps4 Obita, Takayuki; Saksena, Suraj; Ghazi-Tabatabai, Sara Nature, Vol. 449, Issue 7163 https://doi.org/10.1038/nature06171	journal	October 2007
ESCRT-III recognition by VPS4 ATPases Stuchell-Brereton, Melissa D.; Skalicky, Jack J.; Kieffer, Collin Nature, Vol. 449, Issue 7163 https://doi.org/10.1038/nature06172	journal	October 2007
Membrane scission by the ESCRT-III complex Wollert, Thomas; Wunder, Christian; Lippincott-Schwartz, Jennifer Nature, Vol. 458, Issue 7235 https://doi.org/10.1038/nature07836	journal	February 2009
SPG20 is mutated in Troyer syndrome, an hereditary spastic paraplegia Patel, Heema; Cross, Harold; Proukakis, Christos Nature Genetics, Vol. 31, Issue 4 https://doi.org/10.1038/ng937	journal	July 2002
The biogenesis of multivesicular endosomes Gruenberg, Jean; Stenmark, Harald Nature Reviews Molecular Cell Biology, Vol. 5, Issue 4 https://doi.org/10.1038/nrm1360	journal	April 2004
The emerging shape of the ESCRT machinery Williams, Roger L.; Urbé, Sylvie Nature Reviews Molecular Cell Biology, Vol. 8, Issue 5 https://doi.org/10.1038/nrm2162	journal	May 2007
Membrane budding and scission by the ESCRT machinery: it's all in the neck Hurley, James H.; Hanson, Phyllis I. Nature Reviews Molecular Cell Biology, Vol. 11, Issue 8 https://doi.org/10.1038/nrm2937	journal	June 2010
Receptor downregulation and multivesicular-body sorting Katzmann, David J.; Odorizzi, Greg; Emr, Scott D. Nature Reviews Molecular Cell Biology, Vol. 3, Issue 12 https://doi.org/10.1038/nrm973	journal	December 2002
Structural basis for midbody targeting of spastin by the ESCRT-III protein CHMP1B Yang, Dong; Rismanchi, Neggy; Renvoisé, Benoît Nature Structural & Molecular Biology, Vol. 15, Issue 12 https://doi.org/10.1038/nsmb.1512	journal	November 2008
Structural basis for ESCRT-III protein autoinhibition Bajorek, Monika; Schubert, Heidi L.; McCullough, John Nature Structural & Molecular Biology, Vol. 16, Issue 7 https://doi.org/10.1038/nsmb.1621	journal	June 2009
Structural and mechanistic studies of VPS4 proteins Scott, Anna; Chung, Hyo-Young; Gonciarz-Swiatek, Malgorzata The EMBO Journal, Vol. 24, Issue 20 https://doi.org/10.1038/sj.emboj.7600818	journal	September 2005
Structure and ESCRT-III protein interactions of the MIT domain of human VPS4A Scott, A.; Gaspar, J.; Stuchell-Brereton, M. D. Proceedings of the National Academy of Sciences, Vol. 102, Issue 39 https://doi.org/10.1073/pnas.0502165102	journal	September 2005
Release of autoinhibition converts ESCRT-III components into potent inhibitors of HIV-1 budding Zamborlini, A.; Usami, Y.; Radoshitzky, S. R. Proceedings of the National Academy of Sciences, Vol. 103, Issue 50 https://doi.org/10.1073/pnas.0603788103	journal	December 2006
Structural Basis of Molecular Recognition between ESCRT-III-like Protein Vps60 and AAA-ATPase Regulator Vta1 in the Multivesicular Body Pathway Yang, Zhongzheng; Vild, Cody; Ju, Jiaying Journal of Biological Chemistry, Vol. 287, Issue 52 https://doi.org/10.1074/jbc.M112.390724	journal	October 2012
Interactions of the Human LIP5 Regulatory Protein with Endosomal Sorting Complexes Required for Transport Skalicky, Jack J.; Arii, Jun; Wenzel, Dawn M. Journal of Biological Chemistry, Vol. 287, Issue 52 https://doi.org/10.1074/jbc.M112.417899	journal	October 2012
Relief of Autoinhibition Enhances Vta1 Activation of Vps4 via the Vps4 Stimulatory Element Norgan, Andrew P.; Davies, Brian A.; Azmi, Ishara F. Journal of Biological Chemistry, Vol. 288, Issue 36 https://doi.org/10.1074/jbc.M113.494112	journal	July 2013
Vfa1 Binds to the N-terminal Microtubule-interacting and Trafficking (MIT) Domain of Vps4 and Stimulates Its ATPase Activity Vild, Cody J.; Xu, Zhaohui Journal of Biological Chemistry, Vol. 289, Issue 15 https://doi.org/10.1074/jbc.M113.532960	journal	February 2014
The Role of LIP5 and CHMP5 in Multivesicular Body Formation and HIV-1 Budding in Mammalian Cells Ward, Diane McVey; Vaughn, Michael B.; Shiflett, Shelly L. Journal of Biological Chemistry, Vol. 280, Issue 11 https://doi.org/10.1074/jbc.M413734200	journal	January 2005
Recycling of ESCRTs by the AAA-ATPase Vps4 is regulated by a conserved VSL region in Vta1 Azmi, Ishara; Davies, Brian; Dimaano, Christian The Journal of Cell Biology, Vol. 172, Issue 5 https://doi.org/10.1083/jcb.200508166	journal	February 2006
Did2 coordinates Vps4-mediated dissociation of ESCRT-III from endosomes Nickerson, Daniel P.; West, Matthew; Odorizzi, Greg The Journal of Cell Biology, Vol. 175, Issue 5 https://doi.org/10.1083/jcb.200606113	journal	November 2006
Plasma membrane deformation by circular arrays of ESCRT-III protein filaments Hanson, Phyllis I.; Roth, Robyn; Lin, Yuan The Journal of Cell Biology, Vol. 180, Issue 2 https://doi.org/10.1083/jcb.200707031	journal	January 2008
A role for ubiquitin ligases and Spartin/SPG20 in lipid droplet turnover Eastman, Scott W.; Yassaee, Mina; Bieniasz, Paul D. The Journal of Cell Biology, Vol. 184, Issue 6 https://doi.org/10.1083/jcb.200808041	journal	March 2009
Novel Ist1-Did2 Complex Functions at a Late Step in Multivesicular Body Sorting Rue, Sarah M.; Mattei, Sara; Saksena, Suraj Molecular Biology of the Cell, Vol. 19, Issue 2 https://doi.org/10.1091/mbc.E07-07-0694	journal	February 2008
Ist1 Regulates Vps4 Localization and Assembly Dimaano, Christian; Jones, Charles B.; Hanono, Abraham Molecular Biology of the Cell, Vol. 19, Issue 2 https://doi.org/10.1091/mbc.E07-08-0747	journal	February 2008
Essential Role of hIST1 in Cytokinesis Agromayor, Monica; Carlton, Jez G.; Phelan, John P. Molecular Biology of the Cell, Vol. 20, Issue 5 https://doi.org/10.1091/mbc.E08-05-0474	journal	March 2009
Biochemical Analyses of Human IST1 and Its Function in Cytokinesis Bajorek, Monika; Morita, Eiji; Skalicky, Jack J. Molecular Biology of the Cell, Vol. 20, Issue 5 https://doi.org/10.1091/mbc.E08-05-0475	journal	March 2009
Structural Basis of Ist1 Function and Ist1–Did2 Interaction in the Multivesicular Body Pathway and Cytokinesis Xiao, Junyu; Chen, Xiao-Wei; Davies, Brian A. Molecular Biology of the Cell, Vol. 20, Issue 15 https://doi.org/10.1091/mbc.E09-05-0403	journal	August 2009
Assembly of the AAA ATPase Vps4 on ESCRT-III Shestakova, Anna; Hanono, Abraham; Drosner, Stacey Molecular Biology of the Cell, Vol. 21, Issue 6 https://doi.org/10.1091/mbc.E09-07-0572	journal	March 2010
Regulators of Vps4 ATPase Activity at Endosomes Differentially Influence the Size and Rate of Formation of Intralumenal Vesicles Nickerson, Daniel P.; West, Matthew; Henry, Ryan Molecular Biology of the Cell, Vol. 21, Issue 6 https://doi.org/10.1091/mbc.E09-09-0776	journal	March 2010
SPG20 Protein Spartin Is Recruited to Midbodies by ESCRT-III Protein Ist1 and Participates in Cytokinesis Renvoisé, Benoît; Parker, Rell L.; Yang, Dong Molecular Biology of the Cell, Vol. 21, Issue 19 https://doi.org/10.1091/mbc.E09-10-0879	journal	October 2010
Novel Ist1-Did2 Complex Functions at a Late Step in Multivesicular Body Sorting Rue, Sarah M.; Mattei, Sara; Saksena, Suraj Molecular Biology of the Cell, Vol. 19, Issue 2 https://doi.org/10.1091/mbc.e07-07-0694	journal	February 2008
Ist1 Regulates Vps4 Localization and Assembly Dimaano, Christian; Jones, Charles B.; Hanono, Abraham Molecular Biology of the Cell, Vol. 19, Issue 2 https://doi.org/10.1091/mbc.e07-08-0747	journal	February 2008
Essential Role of hIST1 in Cytokinesis Agromayor, Monica; Carlton, Jez G.; Phelan, John P. Molecular Biology of the Cell, Vol. 20, Issue 5 https://doi.org/10.1091/mbc.e08-05-0474	journal	March 2009
Biochemical Analyses of Human IST1 and Its Function in Cytokinesis Bajorek, Monika; Morita, Eiji; Skalicky, Jack J. Molecular Biology of the Cell, Vol. 20, Issue 5 https://doi.org/10.1091/mbc.e08-05-0475	journal	March 2009
Structural Basis of Ist1 Function and Ist1–Did2 Interaction in the Multivesicular Body Pathway and Cytokinesis Xiao, Junyu; Chen, Xiao-Wei; Davies, Brian A. Molecular Biology of the Cell, Vol. 20, Issue 15 https://doi.org/10.1091/mbc.e09-05-0403	journal	August 2009
Assembly of the AAA ATPase Vps4 on ESCRT-III Shestakova, Anna; Hanono, Abraham; Drosner, Stacey Molecular Biology of the Cell, Vol. 21, Issue 6 https://doi.org/10.1091/mbc.e09-07-0572	journal	March 2010
Regulators of Vps4 ATPase Activity at Endosomes Differentially Influence the Size and Rate of Formation of Intralumenal Vesicles Nickerson, Daniel P.; West, Matthew; Henry, Ryan Molecular Biology of the Cell, Vol. 21, Issue 6 https://doi.org/10.1091/mbc.e09-09-0776	journal	March 2010
SPG20 Protein Spartin Is Recruited to Midbodies by ESCRT-III Protein Ist1 and Participates in Cytokinesis Renvoisé, Benoît; Parker, Rell L.; Yang, Dong Molecular Biology of the Cell, Vol. 21, Issue 19 https://doi.org/10.1091/mbc.e09-10-0879	journal	October 2010
The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function Babst, M. The EMBO Journal, Vol. 17, Issue 11 https://doi.org/10.1093/emboj/17.11.2982	journal	June 1998
Spg20−/− mice reveal multimodal functions for Troyer syndrome protein spartin in lipid droplet maintenance, cytokinesis and BMP signaling Renvoisé, Benoît; Stadler, Julia; Singh, Rajat Human Molecular Genetics, Vol. 21, Issue 16 https://doi.org/10.1093/hmg/dds191	journal	May 2012
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Structure/Function Analysis of Four Core ESCRT-III Proteins Reveals Common Regulatory Role for Extreme C-Terminal Domain Shim, Soomin; Kimpler, Lisa A.; Hanson, Phyllis I. Traffic, Vol. 8, Issue 8 https://doi.org/10.1111/j.1600-0854.2007.00584.x	journal	June 2007
Parallels Between Cytokinesis and Retroviral Budding: A Role for the ESCRT Machinery Carlton, J. G.; Martin-Serrano, J. Science, Vol. 316, Issue 5833 https://doi.org/10.1126/science.1143422	journal	June 2007
A Role for the ESCRT System in Cell Division in Archaea Samson, R. Y.; Obita, T.; Freund, S. M. Science, Vol. 322, Issue 5908 https://doi.org/10.1126/science.1165322	journal	December 2008
ESCRT Machinery Is Required for Plasma Membrane Repair Jimenez, A. J.; Maiuri, P.; Lafaurie-Janvore, J. Science, Vol. 343, Issue 6174 https://doi.org/10.1126/science.1247136	journal	January 2014
Membrane Fission Reactions of the Mammalian ESCRT Pathway McCullough, John; Colf, Leremy A.; Sundquist, Wesley I. Annual Review of Biochemistry, Vol. 82, Issue 1 https://doi.org/10.1146/annurev-biochem-072909-101058	journal	June 2013
THE ESCRT COMPLEXES: Structure and Mechanism of a Membrane-Trafficking Network Hurley, James H.; Emr, Scott D. Annual Review of Biophysics and Biomolecular Structure, Vol. 35, Issue 1 https://doi.org/10.1146/annurev.biophys.35.040405.102126	journal	June 2006
Retrovirus Budding Morita, Eiji; Sundquist, Wesley I. Annual Review of Cell and Developmental Biology, Vol. 20, Issue 1 https://doi.org/10.1146/annurev.cellbio.20.010403.102350	journal	November 2004
A dominant negative form of the AAA ATPase SKD1/VPS4 impairs membrane trafficking out of endosomal/lysosomal compartments: class E vps phenotype in mammalian cells Fujita, H. Journal of Cell Science, Vol. 116, Issue 2 https://doi.org/10.1242/jcs.00213	journal	December 2002

Cited By (8)

Reverse-topology membrane scission by the ESCRT proteins Schöneberg, Johannes; Lee, Il-Hyung; Iwasa, Janet H. Nature Reviews Molecular Cell Biology, Vol. 18, Issue 1 https://doi.org/10.1038/nrm.2016.121	journal	October 2016
MAPT/Tau accumulation represses autophagy flux by disrupting IST1-regulated ESCRT-III complex formation: a vicious cycle in Alzheimer neurodegeneration Feng, Qiong; Luo, Yu; Zhang, Xiang-Nan Autophagy https://doi.org/10.1080/15548627.2019.1633862	journal	June 2019
Overgrazing induces alterations in the hepatic proteome of sheep (Ovis aries): an iTRAQ-based quantitative proteomic analysis Ren, Weibo; Hou, Xiangyang; Wang, Yuqing Proteome Science, Vol. 15, Issue 1 https://doi.org/10.1186/s12953-016-0111-z	journal	December 2016
CHMP1B is a target of USP8/UBPY regulated by ubiquitin during endocytosis Crespo-Yàñez, Xènia; Aguilar-Gurrieri, Carmen; Jacomin, Anne-Claire PLOS Genetics, Vol. 14, Issue 6 https://doi.org/10.1371/journal.pgen.1007456	journal	June 2018
Aquaporin Protein-Protein Interactions Roche, Jennifer; Törnroth-Horsefield, Susanna International Journal of Molecular Sciences, Vol. 18, Issue 11 https://doi.org/10.3390/ijms18112255	journal	October 2017
MAPT/Tau accumulation represses autophagy flux by disrupting IST1-regulated ESCRT-III complex formation: a vicious cycle in Alzheimer neurodegeneration Feng, Qiong; Luo, Yu; Zhang, Xiang-Nan Taylor & Francis https://doi.org/10.6084/m9.figshare.8306372	text	January 2019
MAPT/Tau accumulation represses autophagy flux by disrupting IST1-regulated ESCRT-III complex formation: a vicious cycle in Alzheimer neurodegeneration Feng, Qiong; Luo, Yu; Zhang, Xiang-Nan Taylor & Francis https://doi.org/10.6084/m9.figshare.8306372.v2	text	January 2019
Structural basis of protein translocation by the Vps4-Vta1 AAA ATPase Monroe, Nicole; Han, Han; Shen, Peter S. eLife, Vol. 6 https://doi.org/10.7554/elife.24487	journal	April 2017

Similar Records

Structural basis for midbody targeting of spastin by the ESCRT-III protein CHMP1B

Journal Article · Thu Jan 15 04:00:00 UTC 2009 · Nat. Struct. Mol. Biol. · OSTI ID:1007000

Yang, Dong; Rimanchi, Neggy; Renvoise, Benoit; +3 more

A Novel Mechanism of Regulating the ATPase VPS4 by Its Cofactor LIP5 and the Endosomal Sorting Complex Required for Transport (ESCRT)-III Protein CHMP5

Journal Article · Fri Jan 30 04:00:00 UTC 2015 · Journal of Biological Chemistry · OSTI ID:1229905

Vild, Cody J.; Li, Yan; Guo, Emily Z.; +2 more

The Calpain-7 protease functions together with the ESCRT-III protein IST1 within the midbody to regulate the timing and completion of abscission

Journal Article · Thu Oct 19 04:00:00 UTC 2023 · eLife · OSTI ID:2423944

Paine, Elliott L.; Skalicky, Jack J.; Whitby, Frank G.; +4 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Crystal Structure
Cytokinesis
Endosomal Sorting Complexes Required for Transport (ESCRT)
Hereditary Spastic Paraplegias
IST1
LIP5
Protein Engineering
Protein-Protein Interaction
Spartin
VPS4

Title: Distinct Mechanisms of Recognizing Endosomal Sorting Complex Required for Transport III (ESCRT-III) Protein IST1 by Different Microtubule Interacting and Trafficking (MIT) Domains

Citation Formats

References (62)

Cited By (8)

Similar Records

Related Subjects